Arabidopsis thaliana expresses multiple lines of defense to counterattack Erwinia chrysanthemi

Molecular Plant-Microbe Interactions

Volumn 20, Issue 7, 2007, Pages 794-805

  Fagard, Mathilde ^a   Dellagi, Alia ^a   Roux, Camille ^a   Périno, Claude ^a   Rigault, Martine ^a   Boucher, Virginie ^a   Shevchik, Vladimir E ^b   Expert, Dominique ^a  

^a AGROPARISTECH   (France)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CALLOSE; CYCLOPENTANE DERIVATIVE; ETHYLENE; ETHYLENE DERIVATIVE; GLUCAN; ISOENZYME; JASMONIC ACID; PECTATE LYASE; POLYSACCHARIDE LYASE; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CELL WALL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MUTATION; PECTOBACTERIUM CHRYSANTHEMI; PLANT LEAF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ARABIDOPSIS; BACTERIAL PROTEINS; CELL WALL; CYCLOPENTANES; ETHYLENES; GENE EXPRESSION REGULATION, BACTERIAL; GLUCANS; ISOENZYMES; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; PECTOBACTERIUM CHRYSANTHEMI; PLANT LEAVES; POLYSACCHARIDE-LYASES; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALICYLIC ACID; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); ERWINIA CHRYSANTHEMI;

EID: 34250689490     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-20-7-0794     Document Type: Article

References (79)

1. Adam, L., and Sommerville, S. C. 1996. Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J. 9:341-356.
2. Alonso, J. M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J. R. 1999. EIN2. a bifunctional transducer of ethylene and stress responses in A. thaliana. Science. 284:2148-2152.
3. Bestwick, C. S., Brown, I. R., Bennett, M. H. R., and Mansfield, J. W. 1997. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell 9:209-221.
4. Bouley, J., Condemine, G., and Shevchik, V. E. 2001. The PDZ domain of OutC and the N-terminal region of OutD determine the secretion specificity of the type II Out pathway of E. chrysanthemi. J. Mol. Biol. 308:205-219.
5. Bowles, D. J. 1990. Defense-related proteins in higher plants. Annu. Rev. Biochem. 59:873-907.
6. Bowling, S. A., Clarke, J. D., Liu, Y., Klessig, D. F., and Dong, X. 1997. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell. 9:1573-1584.
7. Broekaert, W. F., Delauré, S. L., De Bolle, M. F. C., and Cammue, B. P. A. 2006. The role of ethylene in host-pathogen interactions. Annu. Rev. Phytopath. 44:393-416.
8. Condemine, G., and Robert-Baudouy, J. 1995. Synthesis and secretion of Erwinia chrysanthemi virulence factors are coregulated. Mol. Plant-Microbe Interact. 8:632-636.
9. Dellagi, A., Rigault, M., Segond, D., Roux, C., Kraepiel, Y., Cellier, F., Briat, J.-F., Gaymard, F., and Expert, D. 2005. Siderophore-mediated upregulation of A. thaliana ferritin expression in response to Erwinia chrysanthemi infection. Plant J. 43:262-272.
10. De Lorenzo, G., Cervone, F., Hahn, M. G., Darvill, A., and Albersheim, P. 1991. Bacterial endopectate lyase: Evidence that plant cell wall pH prevents tissue maceration and increases the half-life of elicitor-active oligogalacturonides. Physiol. Mol. Plant Pathol. 39:335-344.
11. Douet, V., Loiseau, L., Barras F. and Py, B. 2004. Systematic analysis, by the yeast two-hybrid, of protein interaction between components of the type 11 secretory machinery of Erwinia chrysanthemi. Res. Microbiol. 155:71-75.
12. Durrant, W. E., and Dong, X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185-209.
13. Expert, D. 1999. Withholding and exchanging iron: Interactions between Erwinia spp. and their plant hosts. Annu. Rev. Phytopathol. 37:307-334.
14. Favey, S., Labesse, G., Vouille, V., and Boccara, M. 1995. Flavohaemoglobin HmpX: A new pathogenicity determinant in Erwinia chrysanthemi strain 3937. Microbiology. 141:863-871.
15. Franza, T., Mahé, B., and Expert, D. 2005. Erwinia chrysanthemi requires a second iron transport route dependent of the siderophore achromobactin for extracellular growth and plant infection. Mol. Microbiol. 55:261-275.
16. Fujimolo, S. Y. Ohta, M., Usui, A., Shinshi, H., and Ohme-Takagi, M. 2000. A. thaliana ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell. 12:393-404.
17. Gerber, I. B., Zeidler, D., Durner, J., and Dubery, I. A. 2004 Early perception responses of Nicotiana tabacum cells in response to lipopolysaccharides from Burkholderia cepacia. Planta. 218:647-657.
18. Glazebrook, J., Chen W., Estes, B., Chang, H.-R., Nawrath, C., Métraux, J.-P. Zhu, T., and Katagiri, F., 2003. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J. 34:217-228.
19. Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205-227.
20. Govrin, E. M., and Levine, A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10:751-757.
21. Grant, J. J., and Loake, G. J. 2000. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol 124:21-29.
22. Guzman, P., and Ecker, J. R. 1990. Exploiting the triple response of A. thaliana to identify ethylene-related mutants. Plant Cell. 2:513-523.
23. Hassouni, M. E., Chambost, J. P., Expert, D., Van Gijsegem, F., and Barras, F. 1999. The minimal gene set member msrA, encoding peptide methionine sulfoxide reductase, is a virulence determinant of the plant pathogen Erwinia chrysanthemi. Proc. Natl. Acad. Sci. U.S.A. 96:887-892.
24. He, S. Y., Schoedel, C., Chatterjee, A. K., and Collmer, A. 1991. Extracellular secretion of pectate lyase by Erwinia chrysanthemi Out pathway is dependent upon Sec-mediated export across the inner membrane. J. Bacteriol. 173:4310-4317.
25. Jenkins, J., Shevchik, V. E., Hugouvieux-Cotte-Pattat, N., and Pickersgill, R. W. 2004. The crystal structure of pectate lyase Pel9A from Erwinia chrysanthemi. J. Biol. Chem. 279:9139-9145.
26. Jha, G., Rajheshwari, R., and Sonti, R. V. 2005. Bacterial type two secretion system secreted proteins: Double-edged swords for plant-pathogens Mol. Plant-Microbe Interact. 18:891-898.
27. Katagiri, F. 2004. A global view of defense gene expression regulation - a highly interconnected signaling network. Curr. Opin. Plant Biol. 7:506-511.
28. Kazemi-Pour, N., Condemine, G., and Hugouvieux-Cotte-Pattat, N. 2004. The secretome of the plant pathogenic bacterium Erwinia chrysanthemi. Proteomics. 4:3177-3186.
29. Kita, N., Boyd, C. M., Garett, M. R., Jurnak, F., and Keen, N. T. 1996. Differential effect of site-directed mutations in pelC on pectate lyase activity, plant tissue maceration, and elicitor activity. J. Biol. Chem 271:26529-26535.
30. Klessig, D. F., Durner, J., Noad, R., Navarre, D. A., Wendehenne, D., Kumar D., Zhou, J. M., Shah, J., Zhang, S., Kachroo, P., Trifa, Y., Pontier, D., Lam, E., and Silva, H. 2000. Nitric oxide and salicylic acid signaling in plant defense. Proc. Natl. Acad. Sci. U.S.A. 97:8849-8855.
31. Laatu, M., and Condemine, G. 2003. Rhamnogalacturonate lyase RhiE is secreted by the Out system in Erwinia chrysanthemi. J. Bacteriol. 185:1642-1649.
32. La Camera, S., Gouzerh, G., Dhondt, S., Hoffmann L., Fritig, B., Legrand, M., and Heitz, T. 2004. Metabolic reprogramming in plant innate immunity: The contributions of phenylpropanoid and oxylipin pathways. Immunol. Rev. 198:267-284.
33. Lam, E., Kato, N., and Lawton, M. 2001. Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848-853.
34. Lamb, C. and Dixon, R. A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. 48:251-275.
35. Leon, J., Lawton, M. A., and Raskin, I. 1995. Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 108:1673-1678.
36. Lorenzo, O., and Solano, R. 2005. Molecular players regulating the jasmonate signalling network. Curr. Opin. Plant Biol. 8:532-540.
37. Meyer, A., Puhler, A., and Niehaus, K. 2001 The lipopolysaccharides of the phytopathogen Xanthomonas campestris pv. campestris induce an oxidative burst reaction in cell cultures of Nicotiana tabacum. Planta 213:214-222.
38. Métraux, J. P. 2002. Recent breakthroughs in the study of salicylic acid biosynthesis. Trends Plant Sci. 7:332-334.
39. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. U.S.A.
40. Mou, Z., Fan, W., and Dong, X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935-944.
41. Murdoch, L., Corbel, J.-C. Reis, D., Bertheau, Y., and Vian, B. 1999. Differential cell wall degradation by Erwinia chrysanthemi in petiole of Saintpaulia ionantha. Protoplasma 210:59-74
42. Nachin, L., El Hassouni, M., Loiscau, L., Expert, D., and Barras, F. 2001. SoxR-dependent response to oxidative stress and virulence of Erwinia chrysanthemi: The key role of SufC, an orphan ABC ATPase. Mol. Microbiol. 39:960-972.
43. Nachin, L., Loiseau, L., Expert, D., and Barras, F. 2003. SufC; An unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress. EMBO (Eur. Mol. Biol. Organ.) J. 22:427-437.
44. Nawrath, C., and Métraux, J. P. 1999. Salicylic acid induction-deficient mutants of A. thaliana express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell. 11:1393-1404.
45. Norman-Setterblad, C., Vidal, S., and Palva, E, T. 2000. Interacting signal pathways control defense gene expression in A. thaliana in response to cell wall-degrading enzymes from Erwinia carotovora. Mol. Plant-Microbe Interact. 13:430-438.
46. Nurnberger, T., Brunner, F., Kemmerling, B., and Piater, L. 2004. Innate immunity in plants and animals: Striking similarities and obvious differences. Immunol. Rev. 198:249-66.
47. Palva, T. K., Holmström, K.-O., Heino, P., and Palva, E. T. 1993. Induction of plant defense response by exoenzymes of Erwinia carotovora subsp. carotovora. Mol. Plant-Microbe Interact. 6:190-196.
48. Pérombelon, M. C. M. 2002. Potato diseases caused by soft rot erwinias: An overview of pathogenesis. Plant Pathol. 51:1-12.
49. Reymond, P., and Farmer, E. E. 1998. Jasmonate and salicylate as global signals for defense gene expression. Curr. Opin. Plant Biol. 1:404-411.
50. Robert-Baudouy, J., Nasser, W., Condemine, G., Reverchon, S., Shevchik, V. E., and Hugouvieux-Coote-Pattat, N. 2000. Regulation of pectinase gene expression in Erwinia chrysanthemi. Pages 221-268 in: Plant-Microbe Interactions. Vol. 5. G. Stacey and N. T. Keen, eds. American Phytopathological Society Press. St. Paul, MN, U.S.A.
51. Roy, C. Kester, H., Visser, J., Shevchik, V. E., Hugouvieux-Cotte-Pattat, N., Robert-Baudouy, J. and Benen, J. 1999. Modes of action of five different endopectate lyases from Erwinia chrysanthemi 3937. J. Bacteriol. 181:3705-3709.
52. Ryan, C. A., and Farmer, E. E. 1991. Oligosaccharide signals in plants: A current assessment. Annu. Rev. Plant Physiol. Mol. Biol. 42:651-674.
53. Sandkvist, M. 2001. Biology of type II secretion. Mol. Microbiol. 40:271-283.
54. Santos, R., Franza, T., Laporte, M. L., Sauvage, C., Touati, D., and Expert, D. 2001. Essential role of superoxide dismutase on the pathogenicity of Erwinia chrysanthemi strain 3937. Mol. Plant-Microbe Interact. 14:758-767.
55. Scholl, R. L., May S. T., and Ware D. H. 2000. Seed and molecular resources for Arabidopsis. Plant Physiol. 124:1477-80.
56. Shah, J. 2003. The salicylic acid loop in plant defense. Curr. Opin. Plant Biol. 6:365-71.
57. Shevchik, V. E., Robert-Baudouy, J., and Condemine, G. 1997a. Specific interaction between OutD, an Erwinia chrysanthemi outer membrane protein of the general secretory pathway, and secreted proteins. EMBO (Eur. Mol. Biol. Organ.) J 16:3007-3016.
58. Shevchik, V. E., Robert-Baudouy, J., Hugouvieux-Cotte-Pattat, N. 1997b. The pectate lyase Pell of Erwinia chrysanthemi belongs to a new family. J. Bacteriol. 179:7321-7330.
59. Shipton, W. A., and Brown, J. F. 1962. A whole-leaf clearing and staining technique to demonstrate host-pathogen relationships of wheat stem rust. Phytopathology. 52:1313.
60. Shirasu, K., Nakajima, H., Rajasekhar, V. K., Dixon, R. A., and Lamb, C. 1997. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell. 9:261-270.
61. Simons, B. H., Millenaar, F. F., Mulder, L., Van Loon, L. C., and Lambers, H. 1999. Enhanced expression and activation of the alternative oxidase during infection of A. thaliana with Pseudomonas syringae pv. tomato. Plant Physiol. 120:529-538.
62. Smallwood, M., Martin, H., and Knox, J. P. 1995. An epitope of rice threonine- and hydroxyprolinerich glycoprotein is common to cell wall and hydrophobic plasma-membrane glycoproteins. Planta 196:510-522.
63. Staswick, P. E., Su, W., and Howell, S. H. 1992. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an A. thaliana mutant. Proc. Natl. Acad. Sci. U.S.A. 89:6837-6840.
64. Staswick, P. E., Tiryaki, I., and Rowe, M. L. 2002. Jasmonate response locus JAR1 and several related A. thaliana genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405-1415.
65. Sticher, L., Mauch-Mani, B., and Métraux, J.-P. 1997. Systemic acquired resistance. Annu. Rev. Phytopathol. 35:235-70.
66. Summermatter, K., Sticher, L., and Métraux, J. P. 1995. Systemic responses in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv. syringae. Plant Physiol. 108:1379-1385.
67. Thomma, B. P., Eggermont, K., Tierens, K. F., and Broekaert, W. F. 1999. Requirement of functional ethylene-insensitive 2 gene for efficient resistance of A. thaliana to infection by Botrytis cinerea. Plant Physiol. 121:1093-1102.
68. Torres, M. A., Dangl, J. L., and Jones, J. D. 2002. A. thaliana gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. U.S.A. 99:517-522.
69. Torres, M. A., Jones, J. D., and Dangl, J. L. 2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in A. thaliana. Nat. Genet. 37:1130-1134.
70. Torres, M. A., Jones, J. D., and Dangl, J. L. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373-378.
71. Truman, W., de Zabala, M. T., and Grant, M. 2006. Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J. 46:14-33.
72. Van Loon, L. C., Geraats, B. P., and Linthorst, H. J. 2006. Ethylene as a modulator of disease resistance in plants. Trends Plant Sci. 11:184-191.
73. Vasquez-Torres, A., Xu, Y., Jones-Carson, J., Holden, D., Lucia, S. M., Dinauer, M. C., Mastroeni, P., and Fang, F. C. 2000. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287:1655-1658.
74. Venisse, J. S., Gullner, G., and Brisset, M. N. 2001 Evidence for the involvement of an oxidative stress in the initiation of infection of pear by Erwinia amylovora. Plant Physiol. 125:2164-2172.
75. Verwoerd, T. C., Dekker, B. M., and Hoekema, A. 1989. A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17:2362.
76. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. 2001. Isochorismate synthase is required to synthetize salicylic acid for plant defence. Nature 414:562-565.
77. Willats, W. G. T., McCartney, L., Mackie, W., and Knox, J. P. 2001. Pectin: Cell biology and prospects for functional analysis. Plant Mol. Biol. 47:9-27.
78. Xu, L., Liu, P., Lechner, E., Genschik, P., Crosby, W. L., Ma, H., Peng, W., Huang, D., and Xie, D. 2002. The SCF(CO11) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14:1919-35.
79. CAZY (Carbohydrate-Active enZymes) website: afmb.cnrs-mrs.fr/CAZY/